Restoration of orbicularis oculi function by contralateral orbicularis oculi innervated muscle flap vs neuromuscular pedicle technique

EXPERIMENTAL

117,307-312

NEUROLOGY

(1992)

Restoration of Orbicularis Oculi Function by Contralateral Orbicularis Oculi Innervated Muscle Flap vs Neuromuscular Pedicle Technique’ CHARLES H. HOCKMAN? Division

of Basic

Medical

M. DOUGLAS GOSSMAN,'

Sciences, Mercer University University of Louisville,

NORMAN

School of Medicine, Macon, School of Medicine, Louisville,

In preliminary experiments with dogs and cats, unilateral paralysis of the orbicularis oculi muscle group was produced by a section of the seventh nerve that included the posterior auricular branch. Either one of two procedures was then employed in attempts to reinnervate the paralyzed eyelid. In one group of animals, a neuromuscular pedicle was employed and in another, a contralateral orbicularis innervated muscle flap was used. Both methods restored synchronous, reflex blinking to the denervated eyelid. Of the two procedures, neurotization appears to offer the greater promise because the use of a neuromuscular pedicle requires an expendable nerve that is functional, and no such suitable substitute is available in humans. o 1992 Academic Press,

Inc.

INTRODUCTION Paralysis of the facial nerve or its branches may arise from a variety of causes including trauma, infection, ischemia, developmental anomalies, or compression. By far, the most serious consequence of seventh nerve paralysis is loss of ocular protection, a compromise of both voluntary and reflex blinking leading to problems that range from chronic discomfort to permanent visual loss (1). Numerous approaches have been employed to deal with deficits associated with facial nerve paralysis, but restoration of function requires a technique that would promote the transmission of impulses from a functional branch of either facial nerve to the paralyzed muscle group. The recent use of interposition cross-face nerve grafts linking paralyzed facial muscles to branches of the normal contralateral facial nerve have restored a measure of synchronous function to paralyzed facial muscles (21); however, use of this technique has failed to reanimate the orbicularis oculi muscle complex. Alternatives to facial nerve interposition grafts currently in use include cross-cranial nerve grafts such 1 Supported by NIH Grant search to Prevent Blindness, ’ To whom reprint requests

R03 EY06772 and Inc. should be addressed.

a grant

from

Re-

E. LIDDELL,

AND WILLLAM

E. RENEHAN

Georgia 31207; and Department Kentucky 40202-1511

of Ophthalmology,

as the sternomastoid-facial and hypoglossal-facial anastomoses (6, 11). While resting tonus can be restored to all facial muscle groups with these techniques, the sacrifice of a functioning cranial nerve and its muscles is required. Movement is not unconscious and reflexive but must be learned and may be asynchronous. Such procedures often require static support or whole muscle transfer (4, 13, 20). Since few studies have been directed specifically at reinnervation of the orbicularis oculi muscle complex, the development of a reliable technique for the restoration of spontaneous and reflex blinking offers a tremendous challenge (2). Several years ago (22), it was reported that the delayed transfer of the denervated digitorum longus was employed in an attempt to restore reflex blinking. Following the muscle transfer, the extensor tendons were attached to the paralyzed eyelids with the hope that contracture of the transferred muscle would ultimately result in narrowing of the eyelid aperture. The procedure relied upon neurotization of the denervated foot muscle by the normal orbicularis oculi. Although results with this transfer technique were reported as being excellent to satisfactory (23), it has not gained wide acceptance as a solution to orbicularis oculi paralysis. The neurotization concept, whereby a denervated muscle is reinnervated by direct contact with a normal muscle, is attractive in its simplicity. It has been applied with mixed results to reanimation problems in other areas of the face and orbit (9, 10,24), and its use in the present study was based upon observations made during surgery to correct ptosis in a patient. One of us (M.D.G.) found that a strip of orbiciularis oculi muscle could be raised and mobilized by dissection in a temporal to medial direction while still retaining its innervation as judged by testing with electrical stimulation. Furthermore, studies with fresh human cadavers have demonstrated that in many cases motor fibers could be identified coursing through the medial canthal region supplying the upper lid portion of the orbiciularis oculi muscle. The use of a neuromuscular pedicle, a procedure technically more difficult than neurotization, consists of a carefully isolated section of muscle with its motor

307 All

Copyright 0 1992 rights of reproduction

0014-4666192 $5.00 by Academic Press, Inc. in any form reserved.

308

HOCKMAN

FIG. 1. Section of the seventh nerve stylomastoid foramen to produce unilateral laris oculi muscle group.

in the cat as it exits the paralysis of the orbicu-

nerve and nutrient artery dissected free but still attached proximally (see Fig. 2). While not previously applied to the orbicularis oculi, the procedure has been employed in attempts to reinnervate head and neck muscles, especially those of the larynx (1,X, 25,26,27). This technique has also been applied successfully to reinnervate an experimentally denervated lateral rectus muscle in the dog (7). Resting tonus as well as a moderate degree of appropriate movement of the lateral rectus muscle was established in this study. Our objectives in evaluating the neuromuscular pedicle procedure were twofold: (1) to ascertain that the orbicularis oculi muscle could be reinnervated with this technique; and (2) to evaluate the extent to which “nuclear adaptation” would develop, i.e., would a group of motor units normally serving the orbicularis oris muscle, for example, be capable of providing synchronous and appropriate function to the ipsilateral orbicularis muscle group. In the experiments described, both surgical procedures were employed in separate groups of animals. A preliminary account of this investigation has been reported (8).

ET

AL.

FIG. 3. Reinnervation of the paralyzed orbicularis oculi in the cat by neurotization. A narrow strip of orbital and preseptal orbicularis oculi muscle is raised from the side opposite to the paralyzed muscle in the temporal to nasal direction and based in the medial canthal region, and the free end is transposed under the skin and sutured to the exposed orbital portion of the denervated orbicularis oculi muscle.

METHODS

A total of 12 adult animals of both sexes were used in this investigation, 7 cats and 5 dogs. The former weighed between 2.4 and 4.1 kg and the latter between 9.1 and 25 kg. Cats were anesthetized with 22 mg/kg ketamine and 2 mg xylazine, both drugs being given im, and dogs were anesthetized with iv 30 mglkg sodium pentobarbitol. All animals were given atropine to control airway secretions, and patency of the airway during surgery was maintained by endotracheal intubation. The control group consisted of two cats and three dogs. In each cat, one facial nerve was exposed and severed as it exited the stylomastoid foramen. The posterior auricular branch was preserved as illustrated in Fig. 1. Intraoperative stimulation of the distal nerve stump with a Haer Pulsar 4i stimulator confirmed the nerve distribution to the ipsilateral facial muscles. A 2-cm

DONOR-ORRlClJlARlS

FIG. 2. Denervation sion of one facial nerve along with the posterior

in the dog showing and its communicating auricular branch.

that the superior divibranches are severed

ORIS

FIG. 4. Reinnervation in the dog of the paralyzed orbicularis oculi muscle, with a neuromuscular pedicle derived from the inferior portion of the orbicularis oris muscle, translocated and sutured to the denervated ipsilateral orbicularis oculi muscle group.

RESTORATION

FIG.

5.

Unoperated

cat in which

HRP

OF

reaction

ORBICULARIS

product

segment of the nerve was then excised to prevent spontaneous anastomosis, and the wound closed with nylon sutures and covered with Neosporin ointment. In the dogs, the superior division of the facial nerve was removed along with its communicating branches. The posterior auricular branch was preserved in one animal as illustrated in Fig. 2. Wounds were treated as indicated above. Recovery of all animals was carefully monitored in an intensive care area for 24 h after which each animal was examined regularly for the development of unconscious periodic blinking secondary to spontaneous reinnervation. Each animal also underwent periodic neurological testing which included the orbicularis stretch reflex, the cornea1 blink reflex, and blink to a threatening gesture. The cornea was also examined regularly. Results were documented and analyzed by videotaping at regular intervals for 4 to 6 months. Experimental animals were divided into two groups: the first group will be referred to as the Neurotization Group (NG) and the second group as the Neuromuscular Pedicle Group (NPG). In the NG, four cats of both sexes were denervated as described earlier for the control group, and during the

OCULI

309

FUNCTION

is seen in cell bodies

of the facial

nucleus

of the injected

side.

same operative procedure, a narrow strip of orbital and preseptal orbicularis oculi muscle was raised from the contralateral side beginning at the lateral canthus and based in the medial region. The free end was transposed under the skin and sutured to the exposed inferior preseptal area of the denervated orbicularis oculi muscle, and the skin was approximated and sutured as illustrated in Fig. 3. Postoperative care and monitoring were identical to that already described for the control animals. In the NPG, two male mongrel dogs were denervated under conditions similar to those described earlier for the control animals except that the posterior auricular branch was removed in all cases as illustrated in Fig. 2. Intraoperative stimulation confirmed innervation to the inferior portion of the orbicularis oris muscle. During the same procedure, a neuromuscular pedicle derived from this latter muscle group was isolated, translocated, and sutured to the denervated ipsilateral orbicularis oculi muscle group at the midpoint of the eyelid. This is illustrated in Fig. 4. In the two dogs, one neuromuscular pedicle was derived and implanted in the denervated orbicularis oculi muscle group and in the other, two neuromuscular pedicles were implanted, one

310

HOCKMAN

in the inferolateral portion (lateral canthal region) and the other in the inferomedial portion (medial canthal region). These two procedures were used to determine whether any quantitative or qualitative benefit might be obtained from more than one pedicle. Horseradish peroxidase (HRP) studies were performed on all animals to characterize the innervation of the orbicularis oculi by the facial nucleus. The orbicularis oculi muscle group on one side was exposed through a small incision in both upper and lower eyelids, and 10 ~1 of a 30% solution of wheat germ agglutinin-HRP (type IV) conjugate and HRP (type VI), in a 15 ratio, was injected into each exposed muscle. The wound was sutured, neosporin ointment was applied, and the animal was allowed to recover for 4 days. Under deep pentobarbital anesthesia, each animal was perfused through the ascending aorta with phosphate-buffered saline (2 liters for each cat and 4 liters for each dog) to which 1000 U/liter sodium heparin had been added via a cannula inserted through the wall of the left ventricle and past the aortic valve. Simultaneously the superior vena cava was severed to facilitate exsanguination and the descending aorta was clamped to limit perfusion to the upper body. Immediately thereafter, the perfusate was switched to a 1.0% paraformaldehyde, 2.5% glutaraldehyde fixative solution (cats, 1 liter; dogs, 2 liters) and then to 5% sucrose-phosphate buffer (cats, 500 ml; dogs, 1 liter) to improve tissue handling in the subsequent frozen sectioning of the brainstem. The brainstem of each animal was carefully removed and refrigerated overnight in a 5% sucrose-phosphate buffer until processed the following day. Frozen sections 50 microns thick were cut on an American Optical microtome from a Cryo-Histomat MK 2 stage. Staining for HRP was carried out following a slightly modified method of Mesulam (16), utilizing triple distilled water. A Nikon Optiphot microscope equipped with brightfield and darkfield illumination was used to locate the HRP reaction product in the tissue sections. Results were compared with those of Radpour (19) who mapped those loci in the brainstem that controlled the orbicularis oculi muscle group and other facial muscles in the kitten.

RESULTS

In control animals subjected to complete unilateral facial neurectomy, there was no evidence of innervation to the ipsilateral orbicularis oculi muscle group 3 months following the surgical procedure. This was judged by an absence of periodic blinking, the orbicularis oculi stretch reflex, cornea1 blink reflex, or blink to a threatening gesture. Mild keratitis was noted to have developed in these animals which in one case had progressed to anterior stromal scarring. Over the course of 3 to 6 months, animals were observed to have regained

ET

AL.

very weak cornea1 and orbicularis oculi reflexes on the operated side. In animals that composed the NG, reflex blinking of the denervated orbicularis oculi was re-established between the 6th and 10th postoperative weeks. Spontaneous blinking was bilaterally synchronous and produced approximately 50% normal lid excursion on the denervated side. Full lid closure was seen with the orbicularis oculi reflex produced by percussion of the stretched muscle at the lateral canthus. Improvement in the force of the blink, eyelid excursion, and strength of the orbicularis reflex was seen at 3 months. No deficit in function of the contralateral (donor) muscle was noted. In the NPG, reflex blinking was observed by the end of the 10th postoperative week and well established by the end of the 12th week in both dogs. Orbicularis oculi reflex lid excursion on the operated side of the dog that received one neuromuscular pedicle was estimated at about 75% of that on the contralateral side, whereas lid excursion of the dog with two neuromuscular pedicles was 100%. The number of complete, synchronous, spontaneous blinks per minute was reduced about 50% on the operated side in both dogs (two versus four per minute). Keratitis was initially observed in the immediate postoperative period in animals of both experimental groups, but it resolved quickly and did not lead to corneal ulceration and scarring. In an unoperated cat, HRP reaction product was seen in a large number of cell bodies in the facial nucleus of the injected side (Fig. 5) but was absent in other brainstem nuclei. This is in keeping with findings reported by Radpour (19). The results from this initial experiment confirmed ipsilateral control of the orbicularis oculi in an animal that had not been subjected to any experimental procedure and served to verify the consistency of this technique in our hands. No specific labeling with HRP reaction product was found in the ipsilateral facial nucleus of those experimental animals (NG and NPG) that were clinically denervated. In all these animals, the denervation procedure included the posterior auricular branch of the facial nerve. However, light labeling of a few scattered cell bodies was noted in the ipsilateral facial nucleus of the three control animals in which the posterior auricular branch of the facial nerve was intact. Weak cornea1 and orbicularis stretch reflexes had been observed in these animals.

DISCUSSION

A satisfactory model for permanent paralysis of orbicularis oculi muscle group can be produced in dog and cat by a section of the seventh nerve that cludes the posterior auricular branch. Section of the

the the insu-

RESTORATION

OF ORBICULARIS

perior division of the facial nerve compromised orbicularis oculi function in a manner clinically similar to that seen with a total nerve lesion. The apparent spontaneous but incomplete reinnervation of this muscle in animals in the control group may have occurred via the retroauricular branch of the facial nerve that was left intact in these animals. This partial return of function could have occurred directly through the facial nerve since complex plexiform arrangements with multiple anastomoses are known to occur and have been described in humans (5); or it could have occurred through other alternate pathways as suggested by Parnes et al. (18). In view of these many possibilities, we undertook retrograde axonal transport of HRP to determine the brainstem location of the cell bodies of controlling neurons and, as already indicated, no specific labeling with HRP reaction product was found in the brainstem of those animals that were clinically denervated; however, light labeling of scattered cell bodies was noted in the ipsilateral facial nuclei of three animals that had shown weak recovery reflex responses at 6 months after surgery. It will be recalled that these observations were confined to control animals. These experiments demonstrated that synchronous, reflex blinking was restored to the denervated eyelid with both experimental techniques. Results observed in the NPG were comparable to those reported earlier in which neuromuscular pedicles were used to reinnervate extraocular muscles (7) and vocal cords (9). In one experiment, the use of two neuromuscular pedicles produced more forceful and complete closure by the 12th postoperative week than did either a single neuromuscular pedicle or neurotization. Although neurotization restored synchronous, reflex blinking, it did not produce lid closure with so great a force or completeness as that seen with the neuromuscular pedicle; however, it was sufficient to prevent keratitis and possessed blink dynamics superior to that seen in the NPG in terms of synchronization. Of the two procedures, neurotization appears to offer the greater promise because the neuromuscular pedicle technique requires an expendable donor nerve that is functional, and no such suitable substitute is available in humans. Neurotization does not produce a deficit in the donor muscle, is a relatively easier procedure to perform, and appears to produce synchronous, unconscious blinking and adequate cornea1 protection in experimental animals. These results lend support to earlier findings on the use of neuromuscular pedicles and draw attention to this technique and to neurotization as possible methods for reinnervation of the orbicularis oculi muscle group. (Furthermore, experimentation on the long-term viability of the techniques and refinement of the experimental procedure would improve significantly the clinical

OCULI

FUNCTION

applicability of these methods in the treatment enth-nerve disorders.)

311 of sev-

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19. R.ADPOUR, S. 1977. Organization of the facial nerve nucleus in the cat. Laryngoscope 87: 557-574. 20. RUBIN, L. R., G. W. LEE, AND R. L. SIMPSON. 1985. Reanimation of the longstanding partial facial paralysis. Plast. Reconsrr. Surg. 77: 41-49. 21. SKI, M. 1976. Rehabilitation of the face by VII nerve substitution. In U. Fisch, Ed., Facial Nerue Surgery (U. Fisch, Ed.), pp. 243-245. Proc. Third Internat. Symp. on Facial Nerve Surgery, Zurich. 22. THOMPSON, N. 1974. A review of autogenous skeletal muscle grafts and their clinical applications. Clin. Plast. Surg. 1: 349403. 23. THOMPSON, N., AND E. H. GUSTAVON. 1976. The use of neuromuscular free autographs with micorneural anastomosis to restore elevation to the paralyzed angle of the mouth in cases of

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unilateral facial paralysis with an analysis of late results of muscle grafts in the treatment of 103 cases of facial hemiparesis. Chir. Plastica. (Berlin) 3: 165-174. TUCKER, H. M. 1976. Human laryngeal innervation. Luryngoscope 96: 769-779. TUCKER, H. M. 1977. Reinnervation of the unilaterally paralyzed larynx. Ann. Otol. Rhirwl. Laryngol. 86: 789-794. TUCKER, H. 1978. Human laryngeal reinnervation: Long-term experience with the nerve muscle pedicle technique. Loryngoscope 88: 598-604. TUCKER, H. 1979. Reinnervation of the paralyzed larynx: A review. Head Neck Surg. 1: 235-242. TUCKER, H. M., J. HARVEY, AND J. H. OGURA. 1970. Vocal cord re-mobilization in the canine larynx. Arch. Otolmyngol. 92: 530534.